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Molecular Biomimetics: Genetic Synthesis, Assembly, and Formation of Materials Using Peptides

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Molecular Biomimetics: Genetic Synthesis, Assembly, and Formation of Materials Using Peptides tide fabrication and assembly processes take place under ambient and environ- mentally friendly conditions.1–11 Gaining the ability to closely manipulate the Molecular behavior of peptides to fully control materials formation would be a giant leap toward realizing nanometer-scale Biomimetics: building blocks that tailor electronic, opti- cal, mechanical, or magnetic materials properties.25 Molecular biology and genet- ics approaches could modify the polypep- Genetic Synthesis, tides and their molecular-recognition characteristics,11–15 and traditional and state-of-the-art engineering approaches16 could create inorganic or synthetic struc- Assembly, and tures such as nanoparticles,17–20 quantum dots,20 molecular wires21 or nanowires,22 or synthetic molecular systems23 (e.g., organic semiconductors).24 Formation of Proteins are long peptide chains that have diverse properties deriving from the specific amino-acid sequences and the physical chain architectures. The wide Materials Using degree of conformational freedom allows proteins to readily adapt to their environ- ment, and the variability in the genetic Peptides sequence and the conformational freedom gives a protein its crucial functionali- ties.26,27 Proteins inherently have the Candan Tamerler and Mehmet Sarikaya, largest information content among all the biological macromolecules (including Guest Editors DNA, polysaccharides, and lipids). There- fore, proteins are the “machinery” that accomplish a myriad of functions through Abstract their specific recognition and interactions In nature, the molecular-recognition ability of peptides and, consequently, their with biomolecules and that are vital to the functions are evolved through successive cycles of mutation and selection. Using life of single-celled and multicellular biology as a guide, it is now possible to select, tailor, and control peptide–solid organisms.26,27 interactions and exploit them in novel ways. Combinatorial mutagenesis provides a For example, in the biological hard tis- 28 protocol to genetically select short peptides with specific affinity to the surfaces of a sues (Figure 1) in the skeletons of many 29–31 32 variety of materials including metals, ceramics, and semiconductors. In the articles of organisms, in bacterial thin films or 33,34 28 35 this issue, we describe molecular characterization of inorganic-binding peptides; explain nanoparticles (Figure 1a), in cuticles, 29,36 37 their further tailoring using post-selection genetic engineering and bioinformatics; and spines, and spicules (Figure 1b), or 38–40 41 finally demonstrate their utility as molecular synthesizers, erectors, and assemblers. in shells (Figure 1c), biomolecule– The peptides become fundamental building blocks of functional materials, each material interaction is accomplished via 42,43 uniquely designed for an application in areas ranging from practical engineering molecular specificity. This leads to the formation of controlled architectures and to medicine. functions at all scales of dimensional hier- archy.29,44 A more detailed example is mammalian tooth organ.45 In this case, of the six tissues present, four (cementum, Introduction dentin, enamel, and bone) contain a min- Molecular biomimetics is an emerging of designer proteins (such as enzymes) that eral—hydroxyapatite (HA)—as the same key field in science and technology.1 have useful characteristics. The central inorganic component (Figure 1d).46 Through the use of recombinant DNA premise of this interdisciplinary field is Although the HA particles are the major methods, combinatorial approaches have that genetically engineered peptides for component in all hard tissues in tooth,46 as been developed to select and tailor pep- inorganics (GEPIs)1 can be utilized as well as in skeletal bone,47 neither the struc- tides with properties not present in nature. molecular erector sets.2–6 With molecular ture of the individual HA crystallites nor A peptide is two or more amino acids biomimetics methods, peptides may direct their crystallography or overall organiza- linked in a chain. Peptides have desirable synthesis, fabrication, assembly, and archi- tion are the same in any two of these com- inorganic-binding and assembly character- tecture of hybrid materials, creating mate- plex composites, which are particle-filled istics and can be used as molecular build- rials with programmed composition, polymeric nanocomposites.48 Among these ing blocks in practical applications.2–6 The phase, and topology. Such materials could tissues, the enamel of the tooth’s crown peptides work either in isolation or when have designed and controlled functions at provides the hardest material for the body. inserted within the structural framework the molecular or nanometer scale. The pep- Enamel contains almost 99% ceramic 504 MRS BULLETIN • VOLUME 33 • MAY 2008 • www.mrs.org/bulletin Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 27 Sep 2021 at 14:12:35, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1557/mrs2008.102 Molecular Biomimetics: Genetic Synthesis, Assembly, and Formation of Materials Using Peptides trolled molecular-scale organization. Such Magnetotactic Nanomagnetics Hierarchical Structure of molecular-scale control could lead to Bacteria Mammalian Tooth designed functionality with practical implications in a wide range of interdisci- 100 µm plinary fields.1,28,53–55 Examples include E immobilizing nanoinorganic particles on D 1 cm Bulk molecular or solid substrates, developing peptide- based molecular probes, and sur- face engineering of inorganics. If these P Macro developments are accomplished, some of current limitations in molecular technol- 500nm PDL a 50 nm ogy and nanotechnology could be over- C come by bridging dissimilar materials Optical Sponge components with high complexity and assembling molecular and inorganic Spicules nano- components in hybrid systems with B B specific size, shape, and spatial organiza- 10 mm tion.56–60 The biomimetic materials field m 1 mm 200 m Nano 150 nm is now mature enough to address funda- b mental issues at the confluence of materi- Nanomechanics als and biology and to provide practical solutions in engineering and medical fields. This article highlights the selection m 5 m of peptides that bind to solid substrates, the degree of binding, and the use of pep- Micro 1 µm tides as building blocks, and provides a c d guide for future directions. Figure 1. Examples of highly evolved hard tissues from various organisms, controlled by Selection of Inorganic-Binding proteins with engineering functions. (a) Magnetite particles in a magnetotactic bacterium, Peptides Using Combinatorial Aquaspirillum magnetotacticum, form a magnetic compass (from Reference 28). Mutagenesis (b) Spicules of the deep-sea sponge Rosella have optical characteristics comparable to For the last two decades, combinatorial synthetic optical fibers (from Reference 37); a light optical image shows a star-shaped lens biological-display technologies have been at the tip of a spicule, and a secondary electron image shows the fractured surface of a developed for a myriad of biological spicule revealing layered microstructure. (c) The mother-of-pearl of red abalone shell and biotechnological applications. A − (Haliotis Rufescens) has a highly desirable toughness strength combination arising from its biological-display technology is a bacteria unique brick-and-mortar nano-/micro-architecture consisting of CaCO3 platelets in the aragonite phase layered with protein/polysaccharide (from Reference 40). (d) Hierarchical or phage (a virus that infects a bacteria) architecture of the mammalian enamel at the crown of the tooth (from Reference 46). engineered to exhibit a peptide sequence Enamel (E) forms an integrated structure with the dentin (D) underneath at the bulk scale. on the membrane protein of the bacteria The enamel has an architecture of woven enamel rods (3 µm diameter) at the micrometer or on the coat protein of the phage. scale, each rod containing thousands of long HA crystallites (10s of nm thick and several Applications range from the examination mm long), all spatially and crystallographically well-organized on the nanometer scale. of receptor–antibody interactions and the study of protein–ligand interactions to the isolation and directed evolution of material and is a protective cover to the well-integrated transition called the enzymes and proteins for enhanced catal- dental tissues of all mammalians.49 dentin-enamel junction.46,51 Despite the ysis or altered binding characteristics.61–65 HA has a different architecture in each enormous work invested in isolating Among the display technologies, the of the hierarchical scales. The specific many of the proteins and identifying their in vivo selection of peptides using cell- structures are controlled by numerous function in controlling mineralization and surface display (CSD) and phage display proteins such as amelogenin and tuftelin. buildup of tissues and despite the knowl- (PD) has been used most frequently Each of these proteins plays a critical role edge that protein absence leads to genetic (Figure 2).9 CSD is a technology whereby in controlling various structural features diseases such as amelogenin imperfecta,52 a peptides appear on the flagella of a bacte- in the complex, highly evolved, and func- thorough understanding of spatial and rial cell membrane. PD is a technology tional enamel tissue.49,50 During the pro- temporal
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